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Volume 169, Issue 4

Growth rate and nutrient limitation as key drivers of extracellular quorum sensing signal molecule accumulation in Open Access

This article is part of the Environmental Sensing and Cell-Cell Communication collection

Abstract

In , quorum sensing (QS) depends on an interconnected regulatory hierarchy involving the Las, Rhl and Pq systems, which are collectively responsible for the co-ordinated synthesis of a diverse repertoire of -acylhomoserine lactones (AHLs) and 2-alkyl-4-quinolones (AQs). Apparent population density-dependent phenomena such as QS may, however, be due to growth rate and/or nutrient exhaustion in batch culture. Using continuous culture, we show that growth rate and population density independently modulate the accumulation of AHLs and AQs such that the highest concentrations are observed at a slow growth rate and high population density. Carbon source (notably succinate), nutrient limitation (C, N, Fe, Mg) or growth at 25 °C generally reduces AHL and AQ levels, except for P and S limitation, which result in substantially higher concentrations of AQs, particularly AQ -oxides, despite the lower population densities achieved. Principal component analysis indicates that ~26 % variation is due to nutrient limitation and a further 30 % is due to growth rate. The formation of -(3-oxododecanoyl)--homoserine lactone (3OC12-HSL) turnover products such as the ring opened form and tetramic acid varies with the limiting nutrient limitation and anaerobiosis. Differential ratios of -butanoyl-homoserine lactone (C4-HSL), 3OC12-HSL and the AQs as a function of growth environment are clearly apparent. Inactivation of QS by mutation of three key genes required for QS signal synthesis (, and ) substantially increases the concentrations of key substrates from the activated methyl cycle and aromatic amino acid biosynthesis, as well as ATP levels, highlighting the energetic drain that AHL and AQ synthesis and hence QS impose on .

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  • Accepted:
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Keyword(s): 2-alkyl-4-quinolone , continuous culture , growth rate , mass spectrometry , N-acyl-homoserine lactone , nutrient limitation , population density , PQS , Pseudomonas aeruginosa and quorum sensing
Funding
This study was supported by the:
  • Biotechnology and Biological Sciences Research Council (Award BB/R012415/1)
    • Principle Award Recipient: MiguelCámara
  • Biotechnology and Biological Sciences Research Council (Award BB/D007 038/1)
    • Principle Award Recipient: PaulWilliams
  • H2020 Marie Skłodowska-Curie Actions (Award 41376)
    • Principle Award Recipient: Jean-FrédéricDubern
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2023-04-05
2024-05-04
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Growth rate and nutrient limitation as key drivers of extracellular quorum sensing signal molecule accumulation in Pseudomonas aeruginosa
Microbiology 169, 001316 (2023); https://doi.org/10.1099/mic.0.001316
/content/journal/micro/10.1099/mic.0.001316
/content/journal/micro/10.1099/mic.0.001316
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